Brachyura, Grapsidae) That Inhabit the Oyster Reefs of Western Taiwan

Crustaceana 90 (14) 1699-1714

POPULATION STRUCTURE AND FECUNDITY OF TWO SPECIES OF GRAPSID CRABS (BRACHYURA, GRAPSIDAE) THAT INHABIT THE OYSTER REEFS OF WESTERN TAIWAN

KUN-NENG CHEN1), JUNG-TING HSU2) and YIH-TSONG UENG3,4) 1) Department of Electrical Engineering, Kun-Shan University, Tainan City, Taiwan 2) Tainan Hydraulics Laboratory, National Cheng Kung University, Tainan City, Taiwan 3) Department of Environmental Engineering, Kun-Shan University, 195 Kunda Road, Yongkang District, Tainan City, 71070, Taiwan

ABSTRACT

This study on carcinological aspects of oyster farming was carried out at the coast of Yunlin County, Taiwan, for a period of 25 months from July 2012 to July 2014. The space formed by the clustering of the oyster shells provides a habitat for at least eight species of crabs. Nanosesarma minutum was the dominant species (73.7% or n = 18 753) with an average of 59.5 ± 30.6 individuals/string/month, while the average monthly rate of ovigerous females was 12.6 ± 13.0%, and the average number of eggs per berried female was 1510.8 ± 1018.7 eggs/individual. Hemigrapsus penicillatus was the second dominant species (23.9% or n = 6074) with an average of 17.4 ± 17.1 individuals/string/month; here, the average monthly rate of ovigerous female crabs was 4.6 ± 9.0, and the average number of eggs of a berried female was 3073.4 ± 2167.5 eggs/individual.

RÉSUMÉ

Cette étude sur les aspects carcinologiques de la culture d’huître a été effectuée sur la côte du conté de Yunlin, Taiwan, pendant une période de 25 mois de juillet 2012 à juillet 2014. L’espace formé par l’amoncellement des coquilles d’huître a fourni un habitat pour au moins huit espèces de crabe. Nanosesarma minutum a été l’espèce dominante (73,7% ou n = 18 753) avec une moyenne de 59,5 ± 30,6 individus/corde/mois, tandis que le taux moyen mensuel de femelles ovigères était de 12,6 ± 13,0%, et la moyenne d’œufs par femelle était de 1510,8 ± 1018,7 d’œufs/individu. Hemigrapsus penicillatus a été la deuxième espèce dominante (23,9% ou n = 6074) avec une moyenne de 17,4 ± 17,1 individus/corde/mois ; une moyenne mensuelle de femelles ovigères de 4,6 ± 9,0%, et une moyenne de nombre d’œufs par femelle ovigère de 3073,4 ± 2167,5 œufs/individu.

4) Corresponding author; e-mail: [email protected]

INTRODUCTION

Oyster reef communities can provide habitats and change the food webs of aquatic animals in lagoons, estuaries, and intertidal zones. These communities demonstrate the enormous biodiversity of coastal wetlands (Dame et al., 1984, 2001; Newell, 1988; Grabowski & Powers, 2004). Oyster reefs also provide numerous ecosystem services including the production of oysters, maintenance of estuarine water alkalinity, shoreline stabilization, and provision of habitats for fishes and crustaceans (Meyer et al., 1997; Piazza et al., 2005; Tolley & Volety, 2005; Waldbusser & Salisbury, 2014). Crustacea are the most abundant aquatic organisms and are represented by numerous species, exhibiting diverse behaviours and habitats. This diversity in the various groups of crustaceans is a result of their life patterns and reproductive strategies (Sastry, 1983; El-Serehy et al., 2015). Some studies have investigated their size composition, growth, sexual maturity, and life history (Kwei, 1978; Fukui, 1988; Carsen et al., 1996; Doi et al., 2007). Gehrels et al. (2016) reported upon the interaction in predator-prey relationships between mud crabs, Dyspanopeus sayi (Smith, 1869), and green crabs, Carcinus maenas (Linnaeus, 1758). Brousseau & McSweeney (2016) investigated the fecundity and maturation rates of Asian shore crabs, Hemigrapsus sanguineus (De Haan, 1835) and Atlantic mud crabs, Panopeus herbstii H. Milne Edwards, 1834. Although oyster reefs constitute the most threatened coastal habitat because of the regular harvesting of oysters, numerous estuarine and tidal species still provide essential habitats and food resources (Yeager & Layman, 2011). Fecundity is closely related to two biological factors in most crustaceans; it is inversely proportional to egg mass weight and directly proportional to female size (Reid & Corey, 1991; García-Guerrero, 2004; Leme, 2004; Terossi et al., 2010). Fecundity is a key factor in the persistence of a fishery stock and is used to evaluate the status of a population, because it directly affects the recruitment of species in estuarine and marine environments (Begg & Waldman, 1999; Rodrigues et al., 2011). Oyster farming in Taiwan takes approximately 6 months to 1 year from seed to harvest. To illustrate this practice, a common way to farm oysters in Taiwan is by moving the oyster larvae to suitable areas located at coasts and estuaries, using floating frames. The advantage of this method is, that the oysters thus are able to take in nutrients during the whole day, as they are constantly suspended in sea water: they do not fall dry during low tides. Obviously, in this way the oysters can grow faster than when using other farming methods. However, this cultivation method requires harvesting the oysters before the invasion of typhoons, which limits the growth period to around six months a year. By contrast, another prevalent method is to suspend the oyster larvae on the lines on a fixed frame in a

Downloaded from Brill.com10/02/2021 02:39:27PM via free access POPULATION STRUCTURE AND FECUNDITY OF TWO GRAPSID CRABS 1701 lagoon. Due to the cycles of the tides, the oysters will be out of the seawater and be exposed to air twice a day, which results in a slower growth rate compared to the previous method. On the other hand, without the threats of typhoons, the oyster farms in lagoons can extend the cultivation period to one year. During the annual oyster harvest, fishermen remove larger crabs. This man- agement strategy directly changes the life cycle factors of those crabs and indi- rectly affects their populations. To learn the sum of those effects, investigating body size distribution and age composition have provided information, including a forecast of the growth and additional strength of young organisms, as well as possible seasonal variations (Pianka, 1974; Hartnoll & Bryant, 1990; Hsueh, 1991; Czerniejewski & Wawrzyniak, 2006). After the release of eggs, a series of changes in environmental factors can result in a deviation from the normal sex ratio of 1 : 1 (Fisher, 1930; Wilson & Pianka, 1963; Leigh, 1970; Josileen, 2013). Statistical studies have revealed that, of the various relationships, carapace width and fecundity are better indices for the estimation of the reproductive potential of crabs than is body weight (Josileen, 2013). The west coast of Taiwan is an important area for oyster farms, which supply oyster larvae. Oyster farming is a vital economic activity there, and the main species in the oyster farms is Crassostrea angulata (Lamarck, 1819) (cf. Wang et al., 2010; Vaschenko et al., 2013; Hsiao et al., 2016). Oyster reefs are one of the most depleted and degraded marine habitats worldwide (Geraldi et al., 2013), while the income from fisheries is often crucial for rural communities, and the decline and depletion of oyster reefs thus can result in loss of income. This means that sufficient knowledge of the ecosystems built by oyster reefs and farms is important for a sustainable farming strategy, and the crabs that live among the oysters constitute a major component in those ecosystems. Habitat loss is another critical factor contributing to the reduction of fishery resources. The Formosa Plastics Corporation Sixth Naphtha Cracker was established in 1993 at the Jhuoshuei estuary. Before its construction, the area of oyster farms south of the construction area with a water depth < 2 m at low tide was 1212 ha. By 2008, this area was reduced to 1084 ha, with an average annual decrease of 10.7 ha. In addition to reducing the oyster farming area, the habitat for fishery resources was diminished (Chen et al., 2016). However, few studies have analysed the populations and biological patterns of crab species inhabiting oyster farms (Ijeomah et al., 2013). In this study, we investigated the biodiversity, community, and fecundity of crab populations in an oyster culture zone of western Taiwan.

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MATERIAL AND METHODS

The study site of our research was located in the intertidal zone (23°4248N 120°0925E) of Taisi Township, Yunlin County, Taiwan. We set two oyster racks in the study site to simulate oyster farming habitats, and the distance between them was approximately 1 km. We hung ten batches of oyster-shell-strings on the oyster racks with the help of local ﬁshermen once every two weeks, from 2 March 2012 to 12 July 2014. Each oyster-shell-string was composed of a 5-m long plastic rope, tied with 18 empty oyster shells that were spaced evenly along the rope. At high tide, the strings were immersed in the water to a depth of approximately 1-2 m; during low tide, they were exposed for approximately 2 hours/day. The settlement of oyster larvae was possible for 16-20 hours/day. The oyster larvae started to grow after they settled in the empty shells. Hundreds of new live oysters developed on each oyster-shell-string, thereby forming microhabitats for small crabs, barnacles, and mussels.

Sample collection

From July 2012 to July 2014, we procured the crabs that were gathered in oyster reef through collecting the oyster-shell-strings. These oyster-shell-strings had been farmed over a period of 6-12 months, except for the first 3 times. In Taiwan, oysters are often harvested aged older than 6 months, in order to avoid damage during the typhoon season. Local fishermen gathered two oyster-shell- strings from the two oyster racks every two weeks. During collection, we first cut one end of an oyster-shell-string and placed the string into a collection bag (60 × 80 cm, with 1-mm mesh size); we then cut the other end of the string. In the laboratory, we collected the crabs that we found on the oyster shells, and kept them in 75% alcohol. However, on 13 September 2013, drift wood and sand had buried the oyster rack at site B, and thus prevented our retrieval of its strings. Some oyster shells on the oyster-shell-strings collected from the field might detach from the string due to the impact of winter waves. Thus, some strings would present a number of oyster shells of than 18. In such a case, we performed a procedure to normalize the numbers of each type of crab on the oyster-shell-string. For example, when the oyster-shell-string held only 17 shells, then the numbers of crabs were divided by 17 and multiplied by 18. We collected oyster-shell-strings from the study site two to three times per month (for example, we made three collections in August and two in September). Subsequently, we calculated the monthly average number of crabs on each oyster-shell-string.

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Breeding season and reproductive characteristics Each crab specimen collected was identified to the taxonomic species level and next classified into four groups: male, non-berried female, berried female, and juvenile; the numbers of specimens in each group were registered (Dai et al., 1986; Ng et al., 2001). For the two dominant crabs, Nanosesarma minutum (De Man, 1887) and Hemigrapsus penicillatus (De Haan, 1835), measurements were taken to determine their bodily conditions as well as the interrelationships between the values found. For that purpose, we thus determined carapace width (CW; precision = 0.01 mm); total body weight (TW; precision = 0.0001 g); egg mass weight (EW; precision = 0.0001 g), and fecundity (the number of eggs). The minimum carapace width of ovigerous female crabs was estimated to distinguish between adults and juveniles. We then calculated the ratio of EW to TW (EW : TW) (Matsuura et al., 1972; Villegas et al., 1986; Haddon, 1994; Luppi et al., 1997; Secor et al., 2002; García-Guerrero & Hendrickx, 2004). In selecting samples of berried female for counting the number of eggs, some studies have reported a significant loss of eggs during the period of embryonic development (Luppi et al., 1997; Koolkalya et al., 2006). Considering the possibility of egg loss during the sampling process at the study sites and in the transport to the laboratory, we thus had to select ovigerous females carefully, i.e., according to the status of their eggs (Josileen, 2013). The eggs were firmly deposited on the pleopods of the female crabs, and their surface featured a very thin mucosa that exhibited no oozing after depression. Eventually, in the present study, a total of 46 and 32 berried crabs were used for fecundity studies in N. minutum and H. penicillatus, respectively. The data recorded were analysed using subroutines featured in the statistical analysis programs DIVERSE (biodiversity H (log e)), RESEMBLANCE, and SIMPER (PRIMER v.6, PRIMER-E, Plymouth, U.K.) (Krebs, 1999). The results were considered significant when P<0.05. The data are presented as the mean ± standard deviation.

RESULTS

Crab biodiversity and population structure on the oyster reefs During the study period, 54 collections were made from which a total number of 25 442 crabs was procured, comprising nine species from ﬁve families. The biodiversity H (log e) of the total crabs was 0.69. According to table I, four species were dominant. The most dominant was Nanosesarma minutum of the family Grapsidae (subfamily Sesarminae); the number of these crabs collected was 18 753 (73.7% of the total crabs). The second dominant species was Hemigrapsus

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TABLE I Composition of the crab fauna by species in the oyster farms monitored on western Taiwan, in the period July 2012 to July 2014 ∗ Families and species Male Female Juvenile % of total crabs Not berried Ovigerous Camptandriidae Paracleistostoma depressum 69 133 24 42 1.1% De Man, 1895 Grapsidae Hemigrapsus penicillatus 2259 1441 112 2262 23.9% (De Haan, 1835) Nanosesarma minutum 5928 6765 1757 4303 73.7% (De Man, 1887) Pachygrapsus minutus 32– 70.0005% A. Milne-Edwards, 1873 Pilumnidae Pilumnopeus makianus 101 117 13 26 1.0% (Rathbun, 1931) Portunidae Charybdis annulata 17 5 – 8 0.1% (Fabricius, 1798) Thalamita crenata 21– 20.0002% Rüppell, 1830 T. gloriensis Crosnier, 1962 – 1 – – 0.00004% Xanthidae Heteropanope glabra 17 11 1 13 0.2% Stimpson, 1858 Total (individuals) 8396 10 383 6663

∗ Juvenile crabs of N. minutum and H. penicillatus had carapace widths <3.4 and <5.8 mm, respectively. penicillatus also from the Grapsidae (subfamily Varuninae) (n = 6074, 23.9%). The third and fourth most abundant species were, respectively, Paracleistostoma depressum De Man, 1895 (Camptandriidae; n = 268, 1.1%), and Pilumnopeus makianus (Rathbun, 1931) (Pilumnidae; n = 257, 1.0%). Among ovigerous crabs, the minimum carapace widths of N. minutum and H. penicillatus were 3.3 and 5.8 mm, respectively. The carapace widths of juvenile (including young and sub- adult) N. minutum and H. penicillatus were <3.4 and <5.8 mm, respectively. The population structure as determined from the data collected, is presented in table I. After the normalization procedure, each oyster-shell-string was normalized to contain 18 oyster shells, which provided habitats for the crabs. N. minutum was found throughout the year in our collections, with a monthly average of 59.5 ± 30.6 individuals/oyster-shell-string, with a maximum from June to November and a

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Fig. 1. Species composition of crabs in the study area during July 2012 to July 2014. peak in September 2012, i.e., the latter occasion yielding 140.9 individuals/oyster- shell-string, and the ratio of females to males was on average 1.44 : 1 (range: 0.77 : 1 to 2.70 : 1). H. penicillatus was also found throughout the year; its monthly average number was 17.4 ± 17.1 individuals/oyster-shell-string, with a maximum during May to July 2014, and the ratio of females to males was 0.68 : 1 (range: 0.19 : 1 to 3.33 : 1) (fig. 1). The population density of N. minutum was approximately 3.4 times that of H. penicillatus. From July 2012 to July 2013 and from July 2013 to July 2014, the crab populations of the two year-periods monitored showed an average similarity of 61.4%, while during that whole period the average contribution of N. minutum was 64.4% and that of H. penicillatus 35.6%. In the first year period, the monthly average density of N. minutum was 58.1 ± 34.4 individuals/oyster-shell- string (range: 15.4-140.9 individuals) and that of H. penicillatus 16.0 ± 14.3 individuals/oyster-shell-string (0.6-46.5 individuals). In the second year period, the monthly average density of N. minutum was 60.5 ± 26.2 individuals/oyster- shell-string (23.5-110.4 individuals) and that of H. penicillatus 19.7 ± 19.8 individuals/oyster-shell-string (1.7-56.0 individuals). The population densities of N. minutum and H. penicillatus in the first year period were 0.96 and 0.82 times those in the second year period, respectively. In addition, during July 2012 to September 2013, the crab populations of the two sites A and B showed an average similarity of 61.0%, while the average contribution of N. minutum was 71.4% and that of H. penicillatus was 28.6%. At site A, the monthly average density of N. minutum was 172.5 ± 92.6 individuals/oyster-shell-string (range: 42.5-334.5 individuals) and that of H. penicillatus 57.2 ± 56.3 individuals/oyster-shell-string

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Fig. 2. Distribution of crabs at various carapace width (mm) size classes in Nanosesarma minutum (De Man, 1887) and Hemigrapsus penicillatus (De Haan, 1835).

(1.5-179.3 individuals). At site B, the monthly average density of N. minutum was 173.9 ± 98.9 individuals/oyster-shell-string (11.0-318.5 individuals) and that of H. penicillatus 34.4 ± 34.9 individuals/oyster-shell-string (3.0-136.3 individuals). The population densities of N. minutum and H. penicillatus at site A were 0.99 and 1.66 times those at B, respectively. For N. minutum, the average CW of the male was 3.7 ± 1.9 mm (1.1-20.0 mm, n = 581), and that of the female 4.7 ± 2.1 mm (1.1-16.0 mm, n = 716); the maximal CW of N. minutum was 20.0 mm. In H. penicillatus, the average CW of the male was 7.7 ± 2.9 mm (1.1-17.7 mm, n = 300), and that of the female 6.0 ± 2.3 mm (1.5-13.5 mm, n = 328); the maximal CW of H. penicillatus was 17.7 mm. Most specimens of N. minutum and H. penicillatus on the oyster farming reefs were disturbed during the harvesting of oysters, with as a result that their average CW was diminished, i.e., they grew at a slower rate (ﬁg. 2).

Ovigerous season and juvenile crabs; reproductive period The ovigerous season of N. minutum was observed to be from February to September, and the ratio of females to males was 1.44 : 1. The average body TW of ovigerous female crabs was 0.13 ± 0.06 g/female (range: 0.03-0.30 g/female), and the average CW was 6.7 ± 2.1 mm (3.4-12.2 mm, n = 46). The main ovigerous season, however, was from March to May, and it peaked at 39.6% in May 2014. The main season of the recruitment of juvenile crabs (CW < 3.4 mm, including young and sub-adult crabs) was observed to be from May to July, and the juvenile

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Fig. 3. Monthly percentage of ovigerous crabs and percentage of juvenile crabs of Nanosesarma minutum (De Man, 1887) during the study. crabs peaked at 42.6 and 45.3% in May and June 2013, respectively, and at 45.4 and 47.8% in May and July 2014, respectively. When first the ovigerous crabs peaked, then 1-3 months later the juvenile crabs often appeared as a peak in abundance (fig. 3). The ovigerous season of H. penicillatus was observed to be from February to August, and the ratio of females to males was 0.68 : 1. The average body TW of ovigerous female crabs was 0.34 ± 0.19 g/female (range: 0.10-1.12 g/female), and the average CW was 8.9 ± 1.6 mm (5.8-10.8 mm, n = 107). The main ovigerous season, however, was from March to May, and it peaked at 60.0% in April 2014. The main season of juvenile crab (CW < 5.8 mm) recruitment was observed to be from April to July, and the juvenile crabs peaked at 86.3 and 80.3% in April and July 2013, respectively, and at 71.0% in May 2014. When the ovigerous crabs peaked, then 1-2 months later the juvenile crabs often appeared as a peak in abundance (fig. 4). The ratios of juvenile crabs to total crabs for N. minutum and H. penicillatus were approximately the same, but the standard deviation for H. penicillatus was larger.

Fecundity For N. minutum, the average number of eggs of a berried female crab was 1510.8 ± 1018.7 eggs/individual (range: 361-4953 eggs), and the average of EW : TW was 0.17 ± 0.07 (n = 46). For H. penicillatus, the average number of

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Fig. 4. Monthly percentage of ovigerous crabs and percentage of juvenile crabs of Hemigrapsus penicillatus (De Haan, 1835) during the study. eggs of a berried female was 3073.4 ± 2167.5 eggs/individual (759-10 391 eggs), and the average of EW : TW was 0.16 ± 0.08 (n = 32). For P. depressum,the average number of eggs of a berried female crab was 939.7 ± 683.8 eggs/individual (228-1847 eggs), and the average of EW : TW was 0.14 ± 0.07 (n = 5). For P. makianus, the average number of eggs of a berried female crab was 3529 ± 1346 eggs/individual (573-5083 eggs, n = 5), and the average of EW : TW was 0.20 ± 0.03 (0.080-0.238, n =6). The linear relationship found between CW and the number of eggs for N. 2 minutum was FN = 462.81CW − 1789.5(R = 0.8064) and that for H. 2 penicillatus was FH = 958.8CW − 5554.3(R = 0.6891). In addition, the exponential relationship between the CW and the number of eggs for N. minutum 0.2684CW 0.3189CW was FN = 185.46e and that for H. penicillatus was FH = 150.48e (fig. 5). However, the significantly distinct slopes of these two regression equations indicate specific morphometric differences (table II).

DISCUSSION This study yielded information on the realized fecundity of crabs on oyster reefs. Fecundity is expressed as the number of eggs counted, which is related to the CW and total body TW of a female crab and to the weight of the eggs. The fecundity of the large crab Portunus pelagicus (Linnaeus, 1758) was determined to be 60 000-1 976 398, with carapace widths ranging 10-19 cm; and the individual average fecundity of another large crab, Callinectes sapidus

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Fig. 5. Relationship between fecundity and carapace width (mm) for the two dominant species, the grapsids Nanosesarma minutum (De Man, 1887) and Hemigrapsus penicillatus (De Haan, 1835).

Rathbun, 1896 was 2 006 974 ± 991 071, with predominance in CW classes ranging 11-14 cm (Josileen, 2013; Severino-Rodrigues et al., 2013). The ﬁndings for the medium-sized crab Schizophrys aspera (H. Milne Edwards, 1834) indicated that the females had CWs ranging 28-52 mm and fecundities of 2349-13 600 (El- Serehy et al., 2015). Fecundity is often recognized as a crucial parameter for measuring the reproductive output of a species or even of populations (Mantelatto & Fransozo, 1997). The present study revealed that N. minutum was less fecund than H. penicillatus;however, it still was the dominant species in the oyster farms. We presumed that this was due to its higher rate of ovigerous females as well as the higher ratio of females to males, and also to the longer breeding season. In the Suez Canal, Schizophrys aspera also has a low fecundity and a longer breeding season (El-Serehy et al., 2015). Because most berried female crabs on the oyster farming reefs were disturbed during the harvesting of oysters, their CW was small and their fecundity was low (ﬁgs. 2 and 5) (Przemysław & Marcello, 2013). Furthermore, the CW of ovigerous crabs was not normally distributed, and the number of breeding females tended to be lower than that of non-breeding females. After the supplementation of the numbers of individuals in the population by the appearance of the juvenile crabs, the population peaked in 2 months time (Hsueh, 1991). Subsequently, the juvenile crabs bore eggs in their turn. A statistical study of Indian populations of P. pelagicus revealed that, among the various relevant factors, CW and fecundity are more accurate indices for estimating

Downloaded from Brill.com10/02/2021 02:39:27PM via free access 1710 KUN-NENG CHEN, JUNG-TING HSU & YIH-TSONG UENG 5) = n 2.1 0.06 0.25 ± ± ± 1813.5 ( ± (Rathbun, 1931) Pilumnopeus makianus 6) 2403.8 = n 0.07 0.17 0.07 0.54 1.3 10.8 ± ± ± 683.8 ( ± De Man, 1895 Paracleistostoma depressum 3 . 21) 939.7 = 554 n − 2684CW . 0 6891) 7830) 0.08 0.14 9.0 0.19 0.13 1.6 6.2 17.1 . . 0 0 II 46e ± ± ± ± ± 8CW . . = = 2167.5 ( 2 2 185 ± 958 R R ( ( = ABLE (De Haan, 1835) = T H H F F Hemigrapsus penicillatus 5 . 46) 3073.4 1789 = − 2840CW n . 0 8064) 6962) 0.07 0.16 13.0 4.6 2.10.06 8.9 0.34 30.6 17.4 . . 0 0 84e ± ± ± ± ± . 81CW = = . 1018.7 ( 2 2 196 59.5 ± R R 462 ( ( = (De Man, 1887) = N Nanosesarma minutum F N F Parameters of reproductive strategy for four crabs on the oyster reefs in Taiwan (individuals/oyster-shell-string) Linear regression equations Number of eggs of a female 1510 Body wet weight/eggs wet weight 0.17 Month’s ovigerous rate (%) 12.6 CW (mm)TW (g) 6.7 0.13 Parameter Ratio of female to malePopulation density 1.44 : 1 0.68 : 1 2.28 : 1 1.29 : 1 Exponential relationship equations Reproductive months February to September February to August

Downloaded from Brill.com10/02/2021 02:39:27PM via free access POPULATION STRUCTURE AND FECUNDITY OF TWO GRAPSID CRABS 1711 the reproductive potential than is the body TW (Josileen, 2013). The fecundity and size range of P. pelagicus (F = 12 473e0.278CW; CW 10.5-18.9 cm) were 0.2684CW similar to those of N. minutum (FN = 185.46e ;CW6.67± 2.10 mm) 0.3189CW and H. penicillatus (FH = 150.48e ;CW8.93± 1.62 mm) from Taiwan (cf. Josileen, 2013). In Argentina, two euryhaline grapsid crabs, Cyrtograpsus angulatus Dana, 1851 and Chasmagnathus granulata Dana, 1851 [currently referred to as Neohelice granulata (Dana, 1851)], which coexist in a brackish coastal lagoon, had a similar average body size and a similar clutch size (Carsen et al., 1996). For the two grapsid crabs in our study, the relationship between the number of eggs and the female CW can be described using linear regression equations (table II), and was the same as that of brachyuran crabs from Mexico (García-Guerrero & Hendrickx, 2004). However, significantly distinct slopes of the regression equations for these two species indicate specific morphometric differences. These differences are indicated in turn by a markedly higher average egg production in Hemigrapsus, reflecting a proportionally larger volume of the body cavity in relation to CW : TW.

ACKNOWLEDGEMENTS We are grateful to Ms. Yu-Chen Lin, Mr. Po-Ling Deng, Mr. Yi-Hsin Chan, Mr. Yun-Zhan Hsieh, Mr. Bo-Zhi Pan, Mr. Cheng-Hsun Yang, Mr. Feng-Tse Yang, Mr. Ha-Xiang Yang, and Mr. Jin-Lang Lin for ﬁeldwork and data collection. This study was supported by the Tainan Hydraulics Laboratory, National Cheng Kung University, and the Industrial Development Bureau, Ministry of Economic Affairs, ROC (IDB-100-00194650).

REFERENCES

BEGG,G.A.&J.R.WALDMAN, 1999. An holistic approach to fish stock identification. Fish. Res., 43: 35-44. BROUSSEAU,D.J.&L.MCSWEENEY, 2016. A comparison of reproductive patterns and adult dis- persal in sympatric introduced and native marine crabs: implications for species characteristics of invaders. Biol. Invas., 18: 1275-1286. CARSEN,A.E.,S.KLEINMAN &M.A.SCELZO, 1996. Fecundity and relative growth of the crab Platyxanthus patagonicus (Brachyura: Platyxanthidae) in Patagonia, Argentina. J. Crustacean Biol., 16: 748-753. CHEN,K.N.,M.J.CHEN,C.W.TSAO,J.T.HSU,P.-L.DENG &Y.T.UENG, 2016. Seasonal changes in the abundance and composition of fish, crustaceans, and benthos in the Jhuoshuei estuary of western Taiwan. In: H. J. LIN (ed.), 2016 international wetland convention in Taiwan, Taipei: 33-35. CZERNIEJEWSKI,P.&W.WAWRZYNIAK, 2006. Seasonal changes in the population structure of the Chinese mitten crab, Eriocheir sinensis (H. Milne Edwards) in the Odra/Oder estuary. Crustaceana, 79: 1167-1179.

Downloaded from Brill.com10/02/2021 02:39:27PM via free access 1712 KUN-NENG CHEN, JUNG-TING HSU & YIH-TSONG UENG

DAI,A.Y.,S.L.YANG,Y.Z.SONG &G.X.CHEN, 1986. Crabs of the China Sea: i-xi, 1-642, pls. 1-74. [In Chinese.] DAME,R.,D.BUSHEK &T.PRINS, 2001. The role of suspension feeders as ecosystem transformers in shallow coastal environments. In: K. REISE (ed.), The ecology of sedimentary coasts: 11-37. (Springer-Verlag, Berlin). DAME,R.F.,R.G.ZINGMARK &E.HASKIN, 1984. Oyster reefs as processors of estuarine materials. J. Exp. Mar. Biol. Ecol., 83: 239-247. DE HAAN, W., 1835. Crustacea. 60. In: P. F. VON SIEBOLD (ed.), Fauna Japonica. (Muller, Amsterdam). DE MAN, J. G., 1887. Report on the podophthalmous Crustacea of the Mergui Archipelago, collected for the trustees of the Indian Museum, Calcutta, by Dr. John Anderson, F.R.S., superintendant of the museum. Zool. J. Linn. Soc., 22: 1-305. DE MAN, J. G., 1895. Bericht über die von Herrn Schiffscapitän Storm zu Atjeh, an den westlichen Küsten von Malakka, Borneo und Celebes sowie in der Java-See gesammelten Decapoden und Stomatopoden. Zoologische Jahrbücher, Jena (Abteilung für Systematik) 8: 485-609. DOI, W., T. T. LWIN,M.YOKOTA,C.A.STRUSSMANN &S.WATANABE, 2007. Maturity and reproduction of goneplacid crab Carcinoplax vestita (Decapoda, Brachyura) in Tokyo Bay. Fish. Sci., 73: 331-340. EL-SEREHY, H. A., K. A. AL-RASHEID,N.K.IBRAHIM &F.A.AL-MISNED, 2015. Repro- ductive biology of the Suez Canal spider crab Schizophrys aspera (H. Milne Edwards, 1834: Crustacea: Brachyura: Majidae). Saudi J. Biol. Sci., 22: 789-794. FISHER, R. A., 1930. The genetical theory of natural selection: a complete variorum edition. (Oxford University Press, Oxford). FUKUI, Y., 1988. Comparative studies on the life history of the grapsid crabs (Crustacea, Brachyura). Publs Seto Mar. Biol. Lab., 33: 121-162. GARCÍA-GUERRERO,M.&M.E.HENDRICKX, 2004. Fecundity traits of seven species of brachyuran crabs (Decapoda: Brachyura) from the Paciﬁc coast of Mexico. Contrib. Study East Pac. Crustac., 3: 79-85. GEHRELS,H.,K.M.KNYSH,M.BOUDREAU,M.-H.THÉRIAULT,S.C.COURTENAY,R.COX &P.A.QUIJÓN, 2016. Hide and seek: habitat-mediated interactions between European green crabs and native mud crabs in Atlantic Canada. Mar. Biol., Berlin, 163: 152. DOI:10.1007/ s00227-016-2927-6. GRABOWSKI,J.H.&S.P.POWERS, 2004. Habitat complexity mitigates trophic transfer on oyster reefs. Mar. Ecol. Prog. Ser., 277: 291-295. HADDON, M., 1994. Size-fecundity relationships, mating behaviour & larval release in the New Zealand paddle crab, Ovalipes catharus (White, 1843) (Brachyura: Portunidae). New Zeal. J. Mar. Freshw. Res., 28: 329-334. HARTNOLL, R. G. & A. D. BRYANT, 1990. Size-frequency distributions in decapod Crustacea: the quick, the dead & the cast-offs. J. Crustacean Biol., 10: 14-19. HSIAO,S.T.,S.C.CHUANG,K.S.CHEN,P.H.HO,C.L.WU &C.A.CHEN, 2016. DNA barcoding reveals that the common cupped oyster in Taiwan is the Portuguese oyster Crassostrea angulata (Ostreoida; Ostreidae), not C. gigas. Sci. Rep., 6: 34057. DOI:10.1038/ srep34057. HSUEH, S. P. W., 1991. Seasonal occurrence and abundance of brachyuran larvae in a coastal embayment of central California. J. Crustacean Biol., 11: 546-552. JOSILEEN, J., 2013. Fecundity of the blue swimmer crab, Portunus pelagicus (Linnaeus, 1758) (De- capoda, Brachyura, Portunidae) along the coast of Mandapam, Tamil Nadu, India. Crustaceana, 86(1): 48-55. KOOLKALYA,S.,T.THAPANAND,S.TUNKIJJANUJIJ,V.HAVANONT &T.JUTAGATE, 2006. Aspects in spawning biology and migration of the mud crab Scylla olivacea in the Andaman Sea, Thailand. Fish. Manag. Ecol., 13: 391-397.

Downloaded from Brill.com10/02/2021 02:39:27PM via free access POPULATION STRUCTURE AND FECUNDITY OF TWO GRAPSID CRABS 1713

KREBS, C. J., 1999. Ecological methodology (2nd ed.): 1-620. (Benjamin/Cummings, Menlo Park, CA). KWEI, E. A., 1978. Size composition, growth and sexual maturity of Callinectes latimanus (Rath) in two Ghanaian lagoons. Zool. J. Linn. Soc., 64: 151-157. LEIGH,JR., E. G., 1970. Sex ratio and differential mortality between the sexes. Amer. Nat., 104: 205-210. LEME, M. H. A., 2004. Fecundity and fertility of the mangrove crab Sesarma rectum Randall, 1840 (Grapsoidea) from Ubatuba, São Paulo, Brazil. Nauplius, 12: 39-44. LUPPI, T. A., C. C. BAS,E.D.SPIVAK &K.ANGER, 1997. Fecundity of two grapsid crab species in the Laguna Mar Chiquita, Argentina. Arch. Fish. Mar. Res., 45: 149-166. MANTELATTO,F.L.M.&A.FRANSOZO, 1997. Fecundity of the crab Callinectes ornatus Ordway, 1863 (Decapoda, Brachyura, Portunidae) from the Ubatuba region, São Paulo, Brazil. Crustaceana, 70: 214-226. MATSUURA,S.,K.TAKESHITA,H.FUJITA &S.KAWSAKI, 1972. Reproduction and fecundity of the female king crab, Paralithodes camtschatica (Tilesius) in the waters off western Kamchatka. II. Determination of the fecundity based on the counts of the ovarian eggs and of the spawned eggs attached to pleopods. Bull. Far Seas Fish. Res. Lab., 8: 169-190. MEYER,D.L.,E.C.TOWNSEND &G.W.THAYER, 1997. Stabilization and erosion control value of oyster clutch for intertidal marsh. Restoration Ecol., 5: 93-99. NEWELL, R. I., 1988. Ecological changes in Chesapeake Bay: are they the result of overharvesting the American oyster, Crassostrea virginica.In:M.P.LYNCH &E.C.KROME (eds.), Understanding the estuary: advances in Chesapeake Bay research: 536-546. (Chesapeake Research Consortium, Edgewater, MD). NG,P.K.L.,C.H.WANG,P.H.HO &H.T.SHIH, 2001. An annotated checklist of brachyuran crabs from Taiwan (Crustacea: Decapoda). Natl. Taiwan Mus. Spec. Publ. Ser., 11: 86. PIANKA, E. R., 1974. Evolutionary ecology: 1-356. (Harper and Row, New York, NY). PIAZZA,B.P.,P.D.BANKS &M.K.LA PEYRE, 2005. The potential for created oyster shell reefs as a sustainable shoreline protection strategy in Louisiana. Restoration Ecol., 13: 499-506. PRZEMYSŁAW, C. & D. G. MARCELLO, 2013. Realized fecundity in the first brood and size of eggs of Chinese mitten crab (Eriocheir sinensis) — laboratory studies. Int. Res. J. Biol. Sci., 2:1-6. RATHBUN, M. J., 1931. New and rare Chinese crabs. Lingnan Sci. J., 8: 75-125. REID,D.M.&S.COREY, 1991. Comparative fecundity of decapod crustaceans, III. The fecundity of fifty-three species of Decapoda from tropical, subtropical, and boreal waters. Crustaceana, 61: 308-316. RODRIGUES,M.A.,M.F.HEBERLE &F.D’INCAO, 2011. Fecundity variation and abundance of female blue crabs Callinectes sapidus Rathbun, 1896 (Decapoda, Brachyura, Portunidae) in the Patos Lagoon Estuary, RS, Brazil. Atlântica (Rio Grande), 33: 141-148. SASTRY, A. N., 1983. Ecological aspects of reproduction. In: F. J. VERNBERG &W.B.VERNBERG (eds.), The biology of Crustacea: 179-270. (Academic Press, New York, NY). SECOR,D.,A.HINES &A.PLACE, 2002. Japanese hatchery-based stock enhancement: lessons for the Chesapeake Bay blue crab. Special Publication of Maryland Seagrant College Park, Maryland. Publication Number UM-SG-TS-2002-02: 1-44. SEVERINO-RODRIGUES,E.,J.MUSIELLO-FERNANDES,A.A.MOURA,G.M.BRANCO &V.O. CANÉO, 2013. Fecundity, reproductive seasonality and maturation size of Callinectes sapidus females (Decapoda: Portunidae) in the southeast coast of Brazil. Revi. Biol. Trop., 61(2): 595- 602. TEROSSI,M.,L.S.TORATI,I.MIRANDA,M.A.SCELZO &F.L.MANTELATTO, 2010. Comparative reproductive biology of two southwestern Atlantic populations of the hermit crab Pagurus exilis (Crustacea: Anomura: Paguridae). Mar. Ecol., 31: 584-591. TOLLEY, S. G. & A. K. VOLETY, 2005. The role of oysters in habitat use of oyster reefs by resident fishes and decapod crustaceans. J. Shellfish Res., 24: 1007-1012.

Downloaded from Brill.com10/02/2021 02:39:27PM via free access 1714 KUN-NENG CHEN, JUNG-TING HSU & YIH-TSONG UENG

VASCHENKO,M.A.,H.L.HSIEH &V.I.RADASHEVSKY, 2013. Gonadal state of the oyster Crassostrea angulata cultivated in Taiwan. J. Shellfish Res., 32: 471-482. VILLEGAS,C.T.,A.TRINO &R.TRAVINA, 1986. Spawner size and the biological components of the reproduction process in Penaeus monodon Fabricius. In: J. L. MACLEAN &L.V. HOSILLOS (eds.), Proceedings of the first Asian fisheries forum: 701-702. (Asian Fisheries Society, Manila, Philippines). WALDBUSSER,G.G.&J.E.SALISBURY, 2014. Ocean acidification in the coastal zone from an organism’s perspective: multiple system parameters, frequency domains & habitats. Ann. Rev. Mar. Sci., 6: 221-247. WANG,H.,L.QIAN,X.LIU,G.ZHANG &X.GUO, 2010. Classification of a common cupped oyster from southern China. J. Shellfish Res., 29: 857-866. WILSON,M.F.&E.R.PIANKA, 1963. Sexual selection, sex ratio and mating system. Amer. Nat., 97: 405-407. YEAGER,L.A.&C.A.LAYMAN, 2011. Energy flow to two abundant consumers in a subtropical oyster reef food web. Aquatic Ecol., 45: 267-277.

First received 2 February 2017. Final version accepted 26 August 2017.

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